Consequences of Local Conspecific Density Effects for Plant Diversity and Community Dynamics.

Conspecific density dependence (CDD) in plant populations is widespread, most likely caused by local-scale biotic interactions, and has potentially important implications for biodiversity, community composition, and ecosystem processes. However, progress in this important area of ecology has been hindered by differing viewpoints on CDD across subfields in ecology, lack of synthesis across CDD-related frameworks, and misunderstandings about how empirical measurements of local CDD fit within the context of broader ecological theories on community assembly and diversity maintenance. Here, we propose a conceptual synthesis of local-scale CDD and its causes, including species-specific antagonistic and mutualistic interactions. First, we compare and clarify different uses of CDD and related concepts across subfields within ecology. We suggest the use of local stabilizing/destabilizing CDD to refer to the scenario where local conspecific density effects are more negative/positive than heterospecific effects. Second, we discuss different mechanisms for local stabilizing and destabilizing CDD, how those mechanisms are interrelated, and how they cut across several fields of study within ecology. Third, we place local stabilizing/destabilizing CDD within the context of broader ecological theories and discuss implications and challenges related to scaling up the effects of local CDD on populations, communities, and metacommunities. The ultimate goal of this synthesis is to provide a conceptual roadmap for researchers studying local CDD and its implications for population and community dynamics.

Patterns and inferred causes of liana mortality in a tropical forest.

Lianas are major contributors to tropical forest dynamics, yet we know little about their mortality. Using overlapping censuses of the lianas and trees across a 50 ha stand of moist tropical forest, we contrasted community-wide patterns of liana mortality with relatively well-studied patterns of tree mortality to quantify patterns of liana death and identify contributing factors. Liana mortality rates were 172% higher than tree mortality rates, but species-level mortality rates of lianas were similar to trees with 'fast' life-history strategies and both growth forms exhibited similar spatial and size-dependent patterns. The mortality rates of liana saplings (<2.1 cm in diameter), which represent about 50% of liana individuals, decreased with increasing disturbance severity and remained consistently low during post-disturbance stand thinning. In contrast, larger liana individuals and trees of all sizes had elevated mortality rates in response to disturbance and their mortality rates decreased over time since disturbance. Within undisturbed forest patches, liana mortality rates increased with increasing soil fertility in a manner similar to trees. The distinct responses of liana saplings to disturbance appeared to distinguish liana mortality from that of trees, whereas similarities in their patterns of death suggest that there are common drivers of woody plant mortality.

Effects of lianas on forest biogeochemistry during their lives and afterlives.

Climate change and other anthropogenic disturbances are increasing liana abundance and biomass in many tropical and subtropical forests. While the effects of living lianas on species diversity, ecosystem carbon, and nutrient dynamics are receiving increasing attention, the role of dead lianas in forest ecosystems has been little studied and is poorly understood. Trees and lianas coexist as the major woody components of forests worldwide, but they have very different ecological strategies, with lianas relying on trees for mechanical support. Consequently, trees and lianas have evolved highly divergent stem, leaf, and root traits. Here we show that this trait divergence is likely to persist after death, into the afterlives of these organs, leading to divergent effects on forest biogeochemistry. We introduce a conceptual framework combining horizontal, vertical, and time dimensions for the effects of liana proliferation and liana tissue decomposition on ecosystem carbon and nutrient cycling. We propose a series of empirical studies comparing traits between lianas and trees to answer questions concerning the influence of trait afterlives on the decomposability of liana and tree organs. Such studies will increase our understanding of the contribution of lianas to terrestrial biogeochemical cycling, and help predict the effects of their increasing abundance.

Lianas increase lightning-caused disturbance severity in a tropical forest.

Lightning is an important agent of plant mortality and disturbance in forests. Lightning-caused disturbance is highly variable in terms of its area of effect and disturbance severity (i.e. tree damage and death), but we do not know how this variation is influenced by forest structure and plant composition. We used a novel lightning detection system to quantify how lianas influenced the severity and spatial extent (i.e. area) of lightning disturbance using 78 lightning strikes in central Panama. The local density of lianas (measured as liana basal area) was positively associated with the number of trees killed and damaged by lightning, and patterns of plant damage indicated that this occurred because lianas facilitated more electrical connections from large to small trees. Liana presence, however, did not increase the area of the disturbance. Thus, lianas increased the severity of lightning disturbance by facilitating damage to additional trees without influencing the footprint of the disturbance. These findings indicate that lianas spread electricity to damage and kill understory trees that otherwise would survive a strike. As liana abundance increases in tropical forests, their negative effects on tree survival with respect to the severity of lightning-related tree damage and death are likely to increase.

Vessel dimorphism and wood traits in lianas and trees among three contrasting environments.

PREMISE: Determining how xylem vessel diameters vary among plants and across environments gives insights into different water-use strategies among species and ultimately their distributions. Here, we tested the vessel dimorphism hypothesis that the simultaneous occurrence of many narrow and a few wide vessels gives lianas an advantage over trees in seasonally dry environments. METHODS: We measured the diameters of 13,958 vessels from 15 liana species and 10,430 vessels from 16 tree species in a tropical seasonal rainforest, savanna, and subtropical evergreen broadleaved forest. We compared differences in mean and hydraulically weighted vessel diameter (MVD and Dh ), vessel density (VD), theoretical hydraulic conductivity (Kt ), vessel area fraction (VAF), and wood density (WD) between lianas and trees and among three sites. RESULTS: Nine liana species and four tree species had dimorphic vessels. From the tropical seasonal rainforest to the savanna, liana MVD, Dh and Kt decreased, and VD and WD increased, while only tree WD increased. From the tropical seasonal rainforest to the subtropical forest, six wood traits remained unchanged for lianas, while tree MVD, Dh and Kt decreased and VD increased. Trait space for lianas and trees were more similar in the savanna and more divergent in the subtropical forest compared to the tropical seasonal rainforest. CONCLUSIONS: These results suggest that lianas tend to possess greater vessel dimorphism, which may explain how lianas grow well during seasonal drought, influencing their unique distribution across tropical rainfall gradients.

Lianas decelerate tropical forest thinning during succession.

The well-established pattern of forest thinning during succession predicts an increase in mean tree biomass with decreasing tree density. The forest thinning pattern is commonly assumed to be driven solely by tree-tree competition. The presence of non-tree competitors could alter thinning trajectories, thus altering the rate of forest succession and carbon uptake. We used a large-scale liana removal experiment over 7 years in a 60- to 70-year-old Panamanian forest to test the hypothesis that lianas reduce the rate of forest thinning during succession. We found that lianas slowed forest thinning by reducing tree growth, not by altering tree recruitment or mortality. Without lianas, trees grew and presumably competed more, ultimately reducing tree density while increasing mean tree biomass. Our findings challenge the assumption that forest thinning is driven solely by tree-tree interactions; instead, they demonstrate that competition from other growth forms, such as lianas, slow forest thinning and ultimately delay forest succession.

Vegetative phenologies of lianas and trees in two Neotropical forests with contrasting rainfall regimes.

Among tropical forests, lianas are predicted to have a growth advantage over trees during seasonal drought, with substantial implications for tree and forest dynamics. We tested the hypotheses that lianas maintain higher water status than trees during seasonal drought and that lianas maximize leaf cover to match high, dry-season light conditions, while trees are more limited by moisture availability during the dry season. We monitored the seasonal dynamics of predawn and midday leaf water potentials and leaf phenology for branches of 16 liana and 16 tree species in the canopies of two lowland tropical forests with contrasting rainfall regimes in Panama. In a wet, weakly seasonal forest, lianas maintained higher water balance than trees and maximized their leaf cover during dry-season conditions, when light availability was high, while trees experienced drought stress. In a drier, strongly seasonal forest, lianas and trees displayed similar dry season reductions in leaf cover following strong decreases in soil water availability. Greater soil moisture availability and a higher capacity to maintain water status allow lianas to maintain the turgor potentials that are critical for plant growth in a wet and weakly seasonal forest but not in a dry and strongly seasonal forest.

Liana optical traits increase tropical forest albedo and reduce ecosystem productivity.

Lianas are a key growth form in tropical forests. Their lack of self-supporting tissues and their vertical position on top of the canopy make them strong competitors of resources. A few pioneer studies have shown that liana optical traits differ on average from those of colocated trees. Those trait discrepancies were hypothesized to be responsible for the competitive advantage of lianas over trees. Yet, in the absence of reliable modelling tools, it is impossible to unravel their impact on the forest energy balance, light competition, and on the liana success in Neotropical forests. To bridge this gap, we performed a meta-analysis of the literature to gather all published liana leaf optical spectra, as well as all canopy spectra measured over different levels of liana infestation. We then used a Bayesian data assimilation framework applied to two radiative transfer models (RTMs) covering the leaf and canopy scales to derive tropical tree and liana trait distributions, which finally informed a full dynamic vegetation model. According to the RTMs inversion, lianas grew thinner, more horizontal leaves with lower pigment concentrations. Those traits made the lianas very efficient at light interception and significantly modified the forest energy balance and its carbon cycle. While forest albedo increased by 14% in the shortwave, light availability was reduced in the understorey (-30% of the PAR radiation) and soil temperature decreased by 0.5°C. Those liana-specific traits were also responsible for a significant reduction of tree (-19%) and ecosystem (-7%) gross primary productivity (GPP) while lianas benefited from them (their GPP increased by +27%). This study provides a novel mechanistic explanation to the increase in liana abundance, new evidence of the impact of lianas on forest functioning, and paves the way for the evaluation of the large-scale impacts of lianas on forest biogeochemical cycles.

Local canopy disturbance as an explanation for long-term increases in liana abundance.

Canopy disturbance explains liana abundance and distribution within tropical forests and thus may also explain the widespread pattern of increasing liana abundance; however, this hypothesis remains untested. We used a 10-year study (2007-2017) of 117,100 rooted lianas in an old-growth Panamanian forest to test whether local canopy disturbance explains increasing liana abundance. We found that liana density increased 29.2% and basal area 12.5%. The vast majority of these increases were associated with clonal stem proliferation following canopy disturbance, particularly in liana-dense, low-canopy gaps, which had far greater liana increases than did undisturbed forest. Lianas may be ecological niche constructors, arresting tree regeneration in gaps and thus creating a high-light environment that favours sustained liana proliferation. Our findings demonstrate that liana abundance is increasing rapidly and their ability to proliferate via copious clonal stem production in canopy gaps explains much of their increase in this and possibly other tropical forests.

Lianas do not reduce tree biomass accumulation in young successional tropical dry forests.

Young successional tropical forests are crucial in the global carbon cycle because they can quickly sequester large quantities of atmospheric carbon. However, lianas (woody vines) can significantly decrease biomass accumulation in young regenerating forests. Lianas are abundant in tropical dry forests, and thus we hypothesized that lianas reduce biomass accretion in dry forests. Lianas may be particularly detrimental to the growth of young trees, which are vulnerable to competition from lianas. Alternatively, lianas may have a stronger negative effect on the largest trees because lianas seek the high-light environment at the top of the forest canopy. We tested these hypotheses using a liana-removal experiment in 13 dry forest stands that ranged from 1 to 70 years in southwestern Panama. We measured biomass accumulation annually for more than 10,000 stems from 2013 to 2017. Contrary to our expectations, liana removal had no effect on tree biomass accumulation across our successional forests and throughout our study period. Liana removal did not benefit smaller trees or larger trees. Lianas did not increase biomass accumulation on recruits, and did not increase biomass loss due to mortality. Surprisingly, removing lianas had a negative effect on three out of 41 tree species. Lianas had no effect on biomass accumulation and loss, possibly because: (1) trees allocated resources to roots instead of stems, (2) trees and lianas partitioned water, (3) higher irradiance after liana removal reduced soil moisture, or (4) low water availability might have been such a strong stressor that it reduced plant-plant competition.

Allometric scaling laws linking biomass and rooting depth vary across ontogeny and functional groups in tropical dry forest lianas and trees.

There are two theories about how allocation of metabolic products occurs. The allometric biomass partitioning theory (APT) suggests that all plants follow common allometric scaling rules. The optimal partitioning theory (OPT) predicts that plants allocate more biomass to the organ capturing the most limiting resource. Whole-plant harvests of mature and juvenile tropical deciduous trees, evergreen trees, and lianas and model simulations were used to address the following knowledge gaps: (1) Do mature lianas comply with the APT scaling laws or do they invest less biomass in stems compared to trees? (2) Do juveniles follow the same allocation patterns as mature individuals? (3) Is either leaf phenology or life form a predictor of rooting depth? It was found that: (1) mature lianas followed the same allometric scaling laws as trees; (2) juveniles and mature individuals do not follow the same allocation patterns; and (3) mature lianas had shallowest coarse roots and evergreen trees had the deepest. It was demonstrated that: (1) mature lianas invested proportionally similar biomass to stems as trees and not less, as expected; (2) lianas were not deeper-rooted than trees as had been previously proposed; and (3) evergreen trees had the deepest roots, which is necessary to maintain canopy during simulated dry seasons.

Modeling the impact of liana infestation on the demography and carbon cycle of tropical forests.

There is mounting empirical evidence that lianas affect the carbon cycle of tropical forests. However, no single vegetation model takes into account this growth form, although such efforts could greatly improve the predictions of carbon dynamics in tropical forests. In this study, we incorporated a novel mechanistic representation of lianas in a dynamic global vegetation model (the Ecosystem Demography Model). We developed a liana-specific plant functional type and mechanisms representing liana-tree interactions (such as light competition, liana-specific allometries, and attachment to host trees) and parameterized them according to a comprehensive literature meta-analysis. We tested the model for an old-growth forest (Paracou, French Guiana) and a secondary forest (Gigante Peninsula, Panama). The resulting model simulations captured many features of the two forests characterized by different levels of liana infestation as revealed by a systematic comparison of the model outputs with empirical data, including local census data from forest inventories, eddy flux tower data, and terrestrial laser scanner-derived forest vertical structure. The inclusion of lianas in the simulations reduced the secondary forest net productivity by up to 0.46 tC  ha-1  year-1 , which corresponds to a limited relative reduction of 2.6% in comparison with a reference simulation without lianas. However, this resulted in significantly reduced accumulated above-ground biomass after 70 years of regrowth by up to 20 tC /ha (19% of the reference simulation). Ultimately, the simulated negative impact of lianas on the total biomass was almost completely cancelled out when the forest reached an old-growth successional stage. Our findings suggest that lianas negatively influence the forest potential carbon sink strength, especially for young, disturbed, liana-rich sites. In light of the critical role that lianas play in the profound changes currently experienced by tropical forests, this new model provides a robust numerical tool to forecast the impact of lianas on tropical forest carbon sinks.

Semi-automatic extraction of liana stems from terrestrial LiDAR point clouds of tropical rainforests.

Lianas are key structural elements of tropical forests having a large impact on the global carbon cycle by reducing tree growth and increasing tree mortality. Despite the reported increasing abundance of lianas across neotropics, very few studies have attempted to quantify the impact of lianas on tree and forest structure. Recent advances in high resolution terrestrial laser scanning (TLS) systems have enabled us to quantify the forest structure, in an unprecedented detail. However, the uptake of TLS technology to study lianas has not kept up with the same pace as it has for trees. The slower technological adoption of TLS to study lianas is due to the lack of methods to study these complex growth forms. In this study, we present a semi-automatic method to extract liana woody components from plot-level TLS data of a tropical rainforest. We tested the method in eight plots from two different tropical rainforest sites (two in Gigante Peninsula, Panama and six in Nouragues, French Guiana) along an increasing gradient of liana infestation (from plots with low liana density to plots with very high liana density). Our method uses a machine learning model based on the Random Forest (RF) algorithm. The RF algorithm is trained on the eigen features extracted from the points in 3D at multiple spatial scales. The RF based liana stem extraction method successfully extracts on average 58% of liana woody points in our dataset with a high precision of 88%. We also present simple post-processing steps that increase the percentage of extracted liana stems from 54% to 90% in Nouragues and 65% to 70% in Gigante Peninsula without compromising on the precision. We provide the entire processing pipeline as an open source python package. Our method will facilitate new research to study lianas as it enables the monitoring of liana abundance, growth and biomass in forest plots. In addition, the method facilitates the easier processing of 3D data to study tree structure from a liana-infested forest.

Testing ecological theory with lianas.

Contents Summary 366 I. Introduction 366 II. Testing ecological theory: effects of the environment on lianas 369 III. A unified explanation for liana distribution and the maintenance of liana diversity 370 IV. Testing ecological theory: effects of lianas on the environment 373 V. Theoretical effects of lianas on forest diversity 375 VI. Lianas and trophic interactions in forests 375 VII. Unresolved challenges in liana ecology 376 VIII. Conclusions 377 Acknowledgements 377 References 377 SUMMARY: Lianas constitute a diverse polyphyletic plant group that is advancing our understanding of ecological theory. Specifically, lianas are providing new insights into the mechanisms that control plant distribution and diversity maintenance. For example, there is now evidence that a single, scalable mechanism may explain local, regional, and pan-tropical distribution of lianas, as well as the maintenance of liana species diversity. The ability to outcompete trees under dry, stressful conditions in seasonal forests provides lianas a growth advantage that, over time, results in relatively high abundance in seasonal forests and low abundance in aseasonal forests. Lianas may also gain a similar growth advantage following disturbance, thus explaining why liana density and diversity peak following disturbance at the local, forest scale. The study of ecology, however, is more than the effect of the environment on organisms; it also includes the effects of organisms on the environment. Considerable empirical evidence now indicates that lianas substantially alter their environment by consuming resources, suppressing tree performance, and influencing emergent properties of forests, such as ecosystem functioning, plant and animal diversity, and community composition. These recent studies using lianas are transcending classical tropical ecology research and are now providing novel insights into fundamental ecological theory.

Lianas reduce carbon accumulation and storage in tropical forests.

Tropical forests store vast quantities of carbon, account for one-third of the carbon fixed by photosynthesis, and are a major sink in the global carbon cycle. Recent evidence suggests that competition between lianas (woody vines) and trees may reduce forest-wide carbon uptake; however, estimates of the impact of lianas on carbon dynamics of tropical forests are crucially lacking. Here we used a large-scale liana removal experiment and found that, at 3 y after liana removal, lianas reduced net above-ground carbon uptake (growth and recruitment minus mortality) by ∼76% per year, mostly by reducing tree growth. The loss of carbon uptake due to liana-induced mortality was four times greater in the control plots in which lianas were present, but high variation among plots prevented a significant difference among the treatments. Lianas altered how aboveground carbon was stored. In forests where lianas were present, the partitioning of forest aboveground net primary production was dominated by leaves (53.2%, compared with 39.2% in liana-free forests) at the expense of woody stems (from 28.9%, compared with 43.9%), resulting in a more rapid return of fixed carbon to the atmosphere. After 3 y of experimental liana removal, our results clearly demonstrate large differences in carbon cycling between forests with and without lianas. Combined with the recently reported increases in liana abundance, these results indicate that lianas are an important and increasing agent of change in the carbon dynamics of tropical forests.

Lianas suppress seedling growth and survival of 14 tree species in a Panamanian tropical forest.

Lianas are a common plant growth form in tropical forests, where they compete intensely with trees, decreasing tree recruitment, growth, and survival. If the detrimental effects of lianas vary significantly with tree species identity, as is often assumed, then lianas may influence tree species diversity and community composition. Furthermore, recent studies have shown that liana abundance and biomass are increasing relative to trees in neotropical forests, which will likely magnify the detrimental effects of lianas and may ultimately alter tree species diversity, relative abundances, and community composition. Few studies, however, have tested the responses of multiple tree species to the presence of lianas in robust, well-replicated experiments. We tested the hypotheses that lianas reduce tree seedling growth and survival, and that the effect of lianas varies with tree species identity. We used a large-scale liana removal experiment in Central Panama in which we planted 14 replicate seedlings of 14 different tree species that varied in shade tolerance in each of 16 80 x 80 m plots (eight liana-removal and eight unmanipulated controls; 3136 total seedlings). Over a nearly two-yr period, we found that tree seedlings survived 75% more, grew 300% taller, and had twice the aboveground biomass in liana-removal plots than seedlings in control plots, consistent with strong competition between lianas and tree seedlings. There were no significant differences in the response of tree species to liana competition (i.e., there was no species by treatment interaction), indicating that lianas had a similar negative effect on all 14 tree species. Furthermore, the effect of lianas did not vary with tree species shade tolerance classification, suggesting that the liana effect was not solely based on light. Based on these findings, recently observed increases in liana abundance in neotropical forests will substantially reduce tree regeneration, but will not significantly alter tropical tree species diversity, relative abundance, or community composition.

Contribution of lianas to plant area index and canopy structure in a Panamanian forest.

Lianas are an important component of tropical forests, where they reduce tree growth, fecundity, and survival. Competition for light from lianas may be intense; however, the amount of light that lianas intercept is poorly understood. We used a large-scale liana-removal experiment to quantify light interception by lianas in a Panamanian secondary forest. We measured the change in plant area index (PAI) and forest structure before and after cutting lianas (for 4 yr) in eight 80 m × 80 m plots and eight control plots (16 plots total). We used ground-based LiDAR to measure the 3-dimensional canopy structure before cutting lianas, and then annually for 2 yr afterwards. Six weeks after cutting lianas, mean plot PAI was 20% higher in control vs. liana removal plots. One yr after cutting lianas, mean plot PAI was ~17% higher in control plots. The differences between treatments diminished significantly 2 yr after liana cutting and, after 4 yr, trees had fully compensated for liana removal. Ground-based LiDAR revealed that lianas attenuated light in the upper- and middle-forest canopy layers, and not only in the upper canopy as was previously suspected. Thus, lianas compete with trees by intercepting light in the upper- and mid-canopy of this forest.

Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest.

The accumulation of species-specific enemies around adults is hypothesized to maintain plant diversity by limiting the recruitment of conspecific seedlings relative to heterospecific seedlings. Although previous studies in forested ecosystems have documented patterns consistent with the process of negative feedback, these studies are unable to address which classes of enemies (for example, pathogens, invertebrates, mammals) exhibit species-specific effects strong enough to generate negative feedback, and whether negative feedback at the level of the individual tree is sufficient to influence community-wide forest composition. Here we use fully reciprocal shade-house and field experiments to test whether the performance of conspecific tree seedlings (relative to heterospecific seedlings) is reduced when grown in the presence of enemies associated with adult trees. Both experiments provide strong evidence for negative plant-soil feedback mediated by soil biota. In contrast, above-ground enemies (mammals, foliar herbivores and foliar pathogens) contributed little to negative feedback observed in the field. In both experiments, we found that tree species that showed stronger negative feedback were less common as adults in the forest community, indicating that susceptibility to soil biota may determine species relative abundance in these tropical forests. Finally, our simulation models confirm that the strength of local negative feedback that we measured is sufficient to produce the observed community-wide patterns in tree-species relative abundance. Our findings indicate that plant-soil feedback is an important mechanism that can maintain species diversity and explain patterns of tree-species relative abundance in tropical forests.

Pervasive and strong effects of plants on soil chemistry: a meta-analysis of individual plant 'Zinke' effects.

Plant species leave a chemical signature in the soils below them, generating fine-scale spatial variation that drives ecological processes. Since the publication of a seminal paper on plant-mediated soil heterogeneity by Paul Zinke in 1962, a robust literature has developed examining effects of individual plants on their local environments (individual plant effects). Here, we synthesize this work using meta-analysis to show that plant effects are strong and pervasive across ecosystems on six continents. Overall, soil properties beneath individual plants differ from those of neighbours by an average of 41%. Although the magnitudes of individual plant effects exhibit weak relationships with climate and latitude, they are significantly stronger in deserts and tundra than forests, and weaker in intensively managed ecosystems. The ubiquitous effects of plant individuals and species on local soil properties imply that individual plant effects have a role in plant-soil feedbacks, linking individual plants with biogeochemical processes at the ecosystem scale.